Twostep Dialogue Between the Cladoceran Bosmina And

Limnol. Oceanogr., 55(1), 2010, 403–419 E 2010, by the American Society of Limnology and Oceanography, Inc. Two-step dialogue between the cladoceran Bosmina and invertebrate predators: Induction and natural selection W. Charles Kerfoot1,* and A. Scott McNaught2 Department of Biology, University of Michigan, Ann Arbor, Michigan Abstract Aquatic prey species respond to predators with fast (developmental) and slow (selective) feedbacks. Natural selection is assumed to fashion details of induction and to modify baseline morphology, but only rarely do we catch the slower (multi-generation) process in action. Laboratory experiments with Bosmina detected predator- mediated induction and estimated spine heritability (h2 5 0.2–0.5). Third Sister Lake, Michigan, U.S.A., Bosmina exhibited induction to resident (Mesocyclops) and to two nonresident, neighborhood predators (Epischura and Leptodora). However, the magnitude of induction in Third Sister Lake Bosmina to nonresident predators (Epischura, Leptodora) was muted, when compared with induction and final spine lengths in Epischura–Leptodora lakes. Inadvertent escape of Leptodora into Third Sister Lake in 1987 created a long-term (multiyear), whole-lake experiment, where resident Bosmina populations fell under intense size selection. During the interval, Leptodora suppressed a late-season smaller, short-featured species (B. freyii), favored seasonal expansion of an overwintering long-featured species (B. liederi), and selected for longer features in the latter species. Before local extinction, defensive spines of B. liederi achieved lengths comparable to populations that co-occur with Epischura and Leptodora. Given the isolated and ephemeral nature of lakes, akin to between predators and prey (Tollrian and Harvell 1999; islands, to what degree are species and community Relyea 2002). From the standpoint of the prey species: (1) responses fashioned at the local (resident lake) or regional how often and quickly does the predator–prey inductive (lake district) level? Regional dispersal is receiving attention response evolve; (2) how is it maintained (physical–chemical, (De Meester et al. 2002; Havel and Shurin 2004), yet how developmental, and genetic feedbacks); and (3) how many does the duration of species contact modify predator–prey predators are involved? To answer these questions, we interactions, species persistence, and genetic adjustments require more information about the process of natural (Ricklefs and Schluter 1993; Tilman and Kareiva 1997)? selection in lakes, particulars of developmental and genetic Zooplankton communities are probably best approached responses, and details on neighborhood and historical from a regional metapopulation perspective (Kerfoot et al. ecological interactions. 2004; Leibold and Norberg 2004), because long-term In the mid–1980s, a series of zooplankton translocation survival of species is tied both to dispersal and to local experiments investigated predator–prey relationships at interactions (Shurin and Allen 2001). However, unraveling northeastern and Midwestern U.S. localities (i.e., moving ecological and evolutionary responses at local and regional predators and prey around in different lakes to explore scales requires extended studies, although insight may be food-web and ecological interactions [Kerfoot 1987; aided by fortuitous circumstances. McNaught 1993a,b]). Near the end of the planned manipu- One of the challenges is that predator–prey interactions lations in Third Sister Lake, Michigan, U.S.A., during the are complicated by two levels of response (developmental, summer of 1987, Leptodora inadvertently escaped from selective). Early on, species in the cladoceran genera Daphnia enclosures (McNaught et al. 2004). This highly efficient, and Bosmina were found capable of rapid developmental size-selective predator rapidly increased in abundance, reaction to the presence of predators (Daphnia: Grant and creating a long-term whole-lake experiment. Plankton Bayly 1981; Havel 1985; Bosmina: Kerfoot 1987). Since then, samples from 1987 to 1992 documented that Leptodora the nature of inducible defenses has been investigated from became abundant and differentially depleted small-bodied laboratory, field, and theoretical perspectives (Dodson cladoceran species (McNaught 1993a; McNaught et al. 2004). 1989a; Tollrian and Harvell 1999; Gabriel et al. 2005). Yet For 6 yr after 1992, as Leptodora reached the height of its abundance, Bosmina became locally extinct. When Leptodora there are many unanswered questions about the nature of crashed in the late 1990s, Bosmina reappeared in 1999 and the dialogue played out in ecological and evolutionary time became abundant again by 2004–2007. A sequence of translocation experiments, laboratory and field observations *Corresponding author: [email protected] between 1987 and 2007 allow insight into developmental and selective responses by Bosmina. Present addresses: 1 Lake Superior Ecosystem Research Center and Department of Biological Sciences, Michigan Technological University, Methods Houghton, Michigan 2 Department of Biology, Central Michigan University, Mount Study system and tested hypotheses—North of Ann Pleasant, Michigan Arbor, Michigan, there is a lake district that contains a 403 404 Kerfoot and McNaught antennules protect the antennae, whereas the posterior mucrones protect rotation towards the ventral groove region, through which algae and bacteria are filtered. The early Third Sister Lake translocation experiments were designed to evaluate the relative importance of induction and natural selection in regulating defensive spine length during short-term experiments by challenging resident populations of Bosmina with more effective, nonresident predators. The unintentional escape and colonization of Third Sister Lake by Leptodora provided us an opportunity to see if natural selection over multiple generations by a highly efficient size-selective predator could push responses beyond regular induction norms. We divided the pheno- typic responses into three periods: pre-Leptodora, Lepto- dora, post-Leptodora. Fig. 1. Bosmina liederi from Third Sister Lake, illustrating position of general length (TL, total length; CL, carapace length) Seasonal pelagic sampling—Bosmina morphology and and defensive spine (ML, mucrones length; AL, antennule length) measurements. Mucro sutures and antennule segments are counts abundance was monitored by hauling a 0.3-m-diameter of cell boundaries that make up the terminal spine structures. plankton net (75 mm or 120 mm Nitex) vertically at a 16-m- deep, central station. Larger net tows used to quantify Leptodora abundance (Fig. 2) are discussed in McNaught diverse assemblage of invertebrate predators (McNaught et et al. (2004). All microcrustaceans were preserved in a 5% al. 2004). Two species of invertebrate predators (the formalin solution to which 40 g L21 of sucrose were added. calanoid copepod Epischura lacustris, the cladoceran Around 40 Bosmina were haphazardly removed from each Leptodora kindtii) not previously reported from Third plankton sample and mounted for measurement. Individ- Sister Lake were collected at Whitmore Lake for a series of uals were placed on a glass slide in a 50% glycerin–water experiments. Previous geographic surveys suggested that mixture. Slides were covered with a glass cover-slip and Third Sister Lake would be suitable for both species, measurements were taken under a Zeiss Universal Micro- although the lake was relatively small (McNaught 1993a,b; scope at 5003. Features measured on all individuals Kerfoot et al. 2000). The field experiments were done in included: (1) total body length, (2) number of mucro suspended enclosures (McNaught 1993a,b; McNaught et sutures, (3) length of mucro, (4) number of antennule al. 2004). Community interactions included size-selective segments, and (5) length of the antennule, measured from responses of planktonic communities to fish and inverte- the tooth to the tip (Fig. 1). If the antennule was curved, brate predators (McNaught 1993a,b; McNaught et al. measurements followed the curvature. 2004), whereas trait responses focused on Bosmina spine lengths (Fig. 1) relative to introduced Epischura and Heritability estimates for defensive traits—Reasons for Leptodora. estimating the heritability (h2) of defensive spines were two- Third Sister Lake was also selected because it had a fold. First, this information is important for determining history of limnological investigations. The waterbody is a the magnitude of selective responses, because the selective small (0.04 km2) seepage lake isolated somewhat to the response equals the heritability times the selective differen- south of the northern district as the third kettle-hole in a tial (Lynch and Walsh 1998). Secondly, we wanted to series that straddles Ann Arbor, Michigan (First, Second, emphasize the cost of selective responses (individuals lost) and Third Sister Lakes; McNaught et al. 2004). The lake is during selection relative to the neutral (no mortality) relatively deep (maximum and mean depths of 16.5 m and condition during induction. 7.2 m, respectively), with no permanent surface inlets or Heritability estimates were attempted only on B. liederi, outlets, and is moderately eutrophic (Lehman and Nau- the most abundant species. Electrophoretic and sequencing moski 1986). Water-column stratification occurs in early studies showed that Third Sister Lake has a cryptic two- spring, after a brief mixing period, followed by the species assemblage (Bosmina

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